Best Cases from the AFIP
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1 AFIP ARCHIVES 589 Editor s Note. Everyone who has taken the course in radiologic pathology at the Armed Forces Institute of Pathology (AFIP) remembers bringing beautifully illustrated cases for accession to the Institute. In recent years, the staff of the Department of Radiologic Pathology has judged the best cases by organ system, and recognition is given to the winners on the last day of the class. With each issue of, one or more of these cases are published, written by the winning resident. Radiologicpathologic correlation is emphasized, and the causes of the imaging signs of various diseases are illustrated. Best Cases from the AFIP Cystic Nephroma 1 John K. Hopkins, MB, BCh, BAO Henry W. Giles, Jr, MD Josephine Wyatt-Ashmead, MD Steven A. Bigler, MD History A 16-month-old boy presented to the emergency department with a 1-day history of gross hematuria. The patient s mother reported an initial brownish discoloration to his urine that progressed overnight to small clots in the diaper on six occasions. The patient also had loose stools, was listless, and had a poor appetite. Past medical history was significant only for a small anal fissure at age 7 months. Vital signs were normal, and the patient was afebrile. Physical examination revealed a large, firm, well-defined nontender mass in the right flank. Urinalysis revealed more than 100 red blood cells per high-power field (normal 0 4 red blood cells per high-power field). Abbreviations: CPDN cystic partially differentiated nephroblastoma, MCDK multicystic dysplastic kidney Index terms: Kidney, cysts, Kidney neoplasms, Kidney neoplasms, diagnosis, , , ; 24: Published online /rg From the Departments of Radiology (J.K.H., H.W.G.) and Pathology (J.W.A., S.A.B.), University of Mississippi Medical Center, 2500 N State St, Jackson, MS Received March 14, 2003; revision requested April 16 and received May 21; accepted May 27. All authors have no financial relationships to disclose. Address correspondence to J.K.H. ( jhopkins@jam.rr.com). RSNA, 2004
2 590 March-April 2004 RG f Volume 24 Number 2 Figure 1. (a) Axial contrast-enhanced abdominal CT scan demonstrates a low-attenuation right renal mass with thin septa. (b) CT scan shows multiple cysts that have herniated into the renal pelvis and ureter (arrow). Note the thin lateral claw of enhancing renal parenchyma. Figure 2. (a) Transverse US image of the right renal fossa shows a multicystic mass with thin, echogenic septa in the proximal ureter (arrow). (b) Transverse US image shows mild hydronephrosis (arrow) due to mass effect and ureteral obstruction. Imaging Findings Initially, contrast material enhanced abdominopelvic computed tomography (CT) was used to evaluate the mass. CT showed a well-circumscribed, cm multiloculated mass with multiple enhancing septa arising from and almost completely replacing the right kidney (Fig 1). There was significant mass effect and herniation of multiple cysts into the proximal ureter. The left kidney appeared normal. These findings were consistent with a multilocular cystic renal tumor. Ultrasound (US) performed to further evaluate the renal vasculature and inferior vena cava showed no vascular involvement but helped confirm the presence of a large renal mass consisting of multiple anechoic cysts separated by thin, echogenic septa (Fig 2). Figure 3. Photograph of the cut specimen shows multiple smooth-walled cysts separated by thin, transparent septa. Note the hemorrhagic-necrotic cysts that have herniated into the proximal ureter (arrow).
3 RG f Volume 24 Number 2 Hopkins et al 591 Figures 4, 5. (4) High-power photomicrograph (original magnification, 400; hematoxylin-eosin stain) shows cuboidal epithelial cells lining the cysts. (5) Lower-power photomicrograph (original magnification, 150; hematoxylin-eosin stain) shows multiple cystic spaces with fibrous tissue septa. Pathologic Evaluation The mass was surgically excised with right nephrectomy and partial ureterectomy and the specimen sent to the pathology department for intraoperative evaluation and work-up. The kidney was intact, with attached adipose tissue and portions of the adrenal gland (1.2 g) and proximal ureter (4.5 cm). Most of the kidney parenchyma was replaced with a bubbly mass consisting of thin-walled, translucent cysts that contained clear, watery fluid (Fig 3). The cystic loculations were cm in diameter and under considerable pressure. The renal pelvis and 4 cm of the attached ureter were also distended by the multicystic mass, which was hemorrhagic and appeared necrotic in the ureteral portion. No solid component was identified. The mass was confined to the kidney and the intraluminal ureter with no renal capsule penetration or gross vascular invasion. A small portion of the lower pole of the kidney had more normal-appearing renal parenchyma. The renal hilum contained lymph nodes measuring cm. At microscopic analysis, the cysts were lined with flat to columnar epithelial cells, occasionally producing a hobnail appearance due to the bulging of the nucleus toward the interior of the cyst (Fig 4). Between the cysts, there was loose stroma with spindle-shaped fibroblasts and cells resembling smooth muscle cells (Fig 5). Between the cysts and underneath the capsule were tiny renal tubules and rare immature glomeruli. A few small collections of lymphocytes were scattered throughout the lesion. The lesion contained foci of necrosis and hemorrhage, especially in the ureteral portion. No blastema was identified, and there were no mitotic figures. No microscopic capsular, lymphatic, or vascular invasion was identified. Ten hilar lymph nodes showed prominent reactive follicular lymphoid hyperplasia with germinal centers. Discussion Cystic nephroma is a rare benign renal neoplasm of uncertain cause. The tumor was originally described by Edmunds in 1892 as a cyst adenoma (1), and since then the spectrum of histologic findings and multiple theories of the pathogenesis of cystic nephroma have given rise to many synonymous terms, including benign multilocular cystic nephroma and cystic nephroblastoma. Cystic nephroma is now classified with cystic partially differentiated nephroblastoma (CPDN) as a multilocular cystic renal tumor. Cystic nephroma and CPDN are histologically distinct but anatomically and radiologically identical. In 1989, Joshi and Beckwith (2) proposed modified terminology and refined diagnostic criteria to help differentiate cystic nephroma from CPDN and other cystic renal tumors such as Wilms tumor with cyst formation. The prevalence of this nonfamilial condition is uncertain. Gallo and Penchansky (3) reported cystic nephroma in 2.4% of 165 primary renal neoplasms seen at their institution. Studies have confirmed a biphasic age and sex distribution: Two-thirds of multilocular cystic renal tumors
4 592 March-April 2004 RG f Volume 24 Number 2 occur in a predominately male pediatric population between 3 months and 2 years old; approximately one-third occur in a mostly female population, with a peak in the 5th and 6th decades of life (4,5). There is no association with cysts in other organs and only sporadic association with other congenital anomalies. Presenting symptoms vary with patient age. Children typically present with a painless, progressively enlarging, palpable abdominal or flank mass that has a variable growth rate and may be discovered incidentally. Adults can present with a variety of nonspecific signs and symptoms, including abdominal and flank pain, urinary tract infection, and hypertension. Hematuria, either microscopic or gross, can occur in either group. In a review of 58 patients with multilocular cystic nephroma at the Armed Forces Institute of Pathology, Madewell et al (5) found hematuria to be related to urinary tract infection and, more commonly (as in our patient), to herniation of pedunculated cysts into the renal pelvis. Variable degrees of obstruction of the renal collecting system can occur due to herniation of the tumor, which can lead to urinary tract infection. Cystic nephroma demonstrates gross pathologic features that are indistinguishable from those of CPDN. A well-circumscribed mass with a thick fibrous capsule contains multiple fluidfilled, noncommunicating cystic spaces separated by connective tissue septa. Typically, the mass is solitary, unilateral, and arises from the lower pole (5), although occasionally (as in this case) it may almost completely replace the kidney. Madewell et al (5), whose study population consisted of children 4 years old and younger, found that the mass had a mean size of cm and the locules ranged from a few millimeters to 2.5 cm. Calcification is rare. Necrosis and hemorrhage are uncommon but are usually seen in association with herniation of the tumor into the renal pelvis or ureter, which damages the thin layer of transitional epithelium (5). At microscopic analysis, the locules are lined by flattened cuboidal or slightly protruding epithelial cells. The fibrous septa lack the blastemal or other embryonal elements found in CPDN but may contain well-differentiated renal tubules. Adequate sampling is essential to distinguish between cystic nephroma and CPDN because the blastemal component theoretically portends the risk of Wilms tumor development. Local recurrence with CPDN was reported in a case of incomplete resection (2). To our knowledge, however, there have been no reports of cystic nephroma demonstrating local aggressive behavior or of malignant transformation. Imaging is vital in differentiating cystic nephroma from other cystic renal masses such as Wilms tumor with cyst formation, clear cell sarcoma, cystic variants of mesoblastic nephroma, and cystic renal cell carcinoma. US and CT are the most commonly used imaging modalities in evaluating cystic nephroma and allow preoperative diagnosis, appropriate surgical planning, and patient follow-up. In larger lesions, conventional abdominal radiography may demonstrate a softtissue mass with associated mass effect and displacement of bowel and adjacent structures. Calcification is infrequently seen; occasionally, however, ossification can occur within septa or within the renal capsule. Central or small peripheral curvilinear calcifications can occasionally be seen at the edge of the herniated pelvic portion (6). Banner et al (4) reported one case of dense calcium rings in multiple cysts. At US, the renal origin of a cystic nephroma is confirmed by the claw or beak of normalappearing renal parenchyma at the periphery of the mass, which displaces the collecting system and moves upon respiration. The size of the locules and the amount of stoma present determine the US appearance. Typically, there are multiple anechoic spaces separated by thin, echogenic septa with no solid elements. US better delineates the internal architecture than does CT, especially if the septa are thin and do not enhance vigorously. Despite its cystic nature, cystic nephroma may appear as a complex, echogenic intrarenal mass due to small cysts causing multiple acoustic interfaces with the US beam (7). At CT, the locules are typically slightly hyperattenuating relative to water. Small locules ( 1 cm) or the presence of myxomatous material within the cysts and the close association with the fibrous septa may cause all or part of the mass to appear solid. The septa enhance moderately due to their vascularity but less than the septa in renal cell carcinoma (8). Contrast material does not accumulate in the cysts because they do not communicate with the collecting system. As in this case, herniation of cysts into the renal pelvis and ureter is readily demonstrated at CT. Uson and Melicow (9) postulated that cysts herniate through a rent in the calix created by stretching of the calices due to a sudden increase in intraabdominal
5 RG f Volume 24 Number 2 Hopkins et al 593 pressure in the presence of a tough fibrous renal capsule. Magnetic resonance (MR) imaging of cystic nephroma has been limited due to the rarity of this lesion and, as with our patient, the sufficiency of CT and US for characterizing the mass. Kettritz et al (10) performed multisequential and multiplanar MR imaging in seven patients, and the results confirmed the presence of multilocular cystic renal tumors. The capsule and septa have low signal intensity on T2-weighted MR images, a finding that reflects the presence of fibrotic elements (10,11). Locules have varying signal intensity depending on the protein or blood product content. Thin internal septa typically enhance after gadolinium administration. Herniation into the renal collecting system was confirmed in all patients in the Kettritz series (10). Renal scintigraphy has also played a limited role in the diagnosis of cystic nephroma. A total of six patients in two Armed Forces Institute of Pathology series (3,5) underwent scintigraphy, which demonstrated a defect corresponding to the renal mass. In one patient, faint radiotracer activity was seen within the mass, a finding that suggested uptake of technetium-99m diethylenetriaminepentaacetic acid by the septa (3). Many diverse disease processes may result in a multiloculated renal mass, including cystic neoplasms, unilateral autosomal dominant polycystic kidney disease, and localized cystic disease of the kidney (12,13). Any solid childhood renal neoplasm may undergo hemorrhage and necrosis and look like a multilocular cystic renal tumor. The presence of solid elements excludes cystic nephroma and implies a more aggressive neoplasm. Cyst formation occurs in less than 10% of Wilms tumors, and rarely is the growth pattern predominantly cystic (14). Cystic nephroma can be differentiated from Wilms tumor by the absence of expansile solid masses of nephroblastomatous tissue. To our knowledge, cystic nephroma has not been diagnosed antenatally and does not occur in the neonatal period, observations that help distinguish it from clear cell sarcoma and cystic variants of mesoblastic nephroma. Multicystic dysplastic kidney (MCDK) can be differentiated from cystic nephroma owing to the absence of normally functioning renal parenchyma and to symmetric contrast material excretion at CT by the remaining normally functioning parenchyma in patients in whom a large portion of the kidney has been replaced by cystic nephroma. In MCDK, it is possible to observe an enhancing central core of solid dysplastic tissue, but this enhancement is different from that of normal renal parenchyma. Segmental MCDK may occur in the obstructed moiety (typically the upper pole moiety) in patients with complete ureteral duplication. At imaging, it may be possible to distinguish segmental MCDK from cystic nephroma without evidence of complete duplication. Treatment of cystic nephroma consists of surgical excision, which is curative whether nephrectomy or nephron-sparing surgery with tumor-free margins is performed. In our case, the patient had an uneventful recovery after undergoing complete resection of the cystic nephroma. References 1. Edmunds W. Cystic adenoma of the kidney. Trans Pathol Soc London 1892; 43: Joshi VV, Beckwith JB. Multilocular cyst of the kidney (cystic nephroma) and cystic, partially differentiated nephroblastoma: terminology and criteria for diagnosis. Cancer 1989; 64: Gallo GE, Penchansky L. Cystic nephroma. Cancer 1977; 39: Banner MP, Pollack HM, Chatten J, Witzleben C. Multilocular renal cysts: radiologic-pathologic correlation. AJR Am J Roentgenol 1981; 136: Madewell JE, Goldman SM, Davis CJ, Hartman DS, Feigin DS, Lichtenstein JE. Multilocular cystic nephroma: a radiologic-pathologic correlation of 58 patients. Radiology 1983; 146: Brown RC, Cornell SH, Culp DA. Multilocular renal cyst with diffuse calcification simulating renal cell carcinoma. Radiology 1970; 95: Agrons G, Wagner B, Davidson A, Suarez E. Multilocular cystic renal tumor in children: radiologicpathologic correlation. 1995; 15: Dalla-Palma L, Pozzi-Mucelli F, di Donna A, Pozzi-Mucelli R. Cystic renal tumors: US and CT findings. Urol Radiol 1990; 12: Uson AC, Melicow M. Multilocular cysts of kidney with intrapelvic herniation of daughter cyst: report of 4 cases. J Urol 1963; 89: Kettritz U, Semelka RC, Siegelman ES, Shoenut JP, Mitchell DG. Multilocular cystic nephroma: MR imaging appearance with current techniques, including gadolinium enhancement. J Magn Reson Imaging 1996; 6: Dikengil A, Benson M, Sanders L, Newhouse JH. MRI of multilocular cystic nephroma. Urol Radiol 1988; 10: Hartman DS, Davis CJ, Sanders RC, Johns TT, Smirniotopoulos J, Goldman SM. The multiloculated renal mass: considerations and differential features. 1987; 7: Slywotzky CM, Bosniak MA. Localized cystic disease of the kidney. AJR Am J Roentgenol 2001; 176: Lowe RE, Cohen MD. Computed tomographic evaluation of Wilms tumor and neuroblastoma. 1984; 4:
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